Passive inertial damping improves high-speed gaze stabilization in hoverflies

Gaze stabilization reflexes reduce motion blur and simplify the processing of visual information by keeping the eyes level. These reflexes typically depend on estimates of the rotational motion of the body, head, and eyes, acquired by visual or mechanosensory systems. During rapid movements, there can be insufficient time for sensory feedback systems to estimate rotational motion, and additional mechanisms are required. The solutions to this common problem likely reflect an animal's behavioral repertoire. Here, we examine gaze stabilization in three families of dipteran flies, each with distinctly different flight behaviors. Through frequency response analysis based on tethered-flight experiments, we demonstrate that fast roll oscillations of the body lead to a stable gaze in hoverflies, whereas the reflex breaks down at the same speeds in blowflies and horseflies. Surprisingly, the high-speed gaze stabilization of hoverflies does not require sensory input from the halteres, their low-latency balance organs. Instead, we show how the behavior is explained by a hybrid control system that combines a sensory-driven, active stabilization component mediated by neck muscles, and a passive component which exploits physical properties of the animal's anatomy---the mass and inertia of the head. This solution requires hoverflies to have specializations of the head-neck joint that can be employed during flight. Our comparative study highlights how species-specific control strategies have evolved to support different visually-guided flight behaviors.

Relationship between eye movements and freezing of gait during turning in individuals with Parkinson disease

Background Individuals with Parkinson disease can experience freezing of gait: a sudden, brief episode of an inability to move their feet despite the intention to walk . Since turning is the most sensitive condition to provoke freezing-of-gait episodes, and the eyes typically lead turning, we hypothesize that disturbances in saccadic eye movements are related to freezing-of-gait episodes. Objectives This study explores the relationship between freezing-of-gait episodes and saccadic eye movements for gaze shift and gaze stabilization during turning. Methods We analyzed 277 freezing-of-gait episodes provoked among 17 individuals with Parkinson disease during two conditions: self-selected speed and rapid speed 180-degree turns in alternating directions. Eye movements acquired from electrooculography signals were characterized by the average position of gaze, the amplitude of gaze shifts, and the speed of gaze stabilization. We analyzed these variables before and during freezing-of-gait episodes occurring at the different phase angles of a turn. Results Significant off-track changes of the gaze position were observed almost one 180-degree-turn time before freezing-of-gait episodes. In addition, the speed of gaze stabilization significantly decreased during freezing-of-gait episodes. Conclusions We argue that off-track changes of the gaze position could be a predictor of freezing-of-gait episodes due to continued failure in movement-error correction or an insufficient preparation for eye-to-foot coordination during turning. The decline in the speed of gaze stabilization is large during freezing-of-gait episodes given the slowness or stop of body turning. We argue that this could be evidence for a healthy compensatory system in individuals with freezing-of-gait.

Visuo-vestibular gaze control - conserved subcortical processing

Gaze stabilization compensates for movements of the head or external environment to minimize image blurring, which is critical for visually-guided behaviors. Multisensory information is used to stabilize the visual scene on the retina via the vestibulo-ocular (VOR) and optokinetic (OKR) reflexes. While the organization of neuronal circuits underlying VOR is well described across vertebrates, less is known about the contribution and evolutionary origin of the OKR circuits. Moreover, the integration of these two sensory modalities is still poorly understood. Here, we developed a novel experimental model, the isolated lamprey eye-brain-labyrinth preparation, to analyze the neuronal pathways underlying visuo-vestibular integration which allowed electrophysiological recordings while applying vestibular stimulation using a moving platform, coordinated with visual stimulation via two screens. We show that lampreys exhibit robust visuo-vestibular integration, with optokinetic information processed in the pretectum and integrated with vestibular inputs at several subcortical levels. The enhanced eye movement response to multimodal stimulation favored the vestibular response at increased velocities. The optokinetic signals can be downregulated from tectum. Additionally, saccades are present in the form of nystagmus. The lamprey represents the oldest living group of vertebrates, thus all basic components of the visuo-vestibular control of gaze were present already at the dawn of vertebrate evolution.

Role of the Trace Amine Associated Receptors 5 (TAAR5) in Sensorimotor Functions

Monoamines are critical modulators of the sensorimotor neural networks. Using trace amine associated receptor 5 (TAAR5) knockout mice that express beta-galactosidase marker, we observed TAAR5 expression in the medial vestibular nucleus and Purkinje cells in the cerebellum suggesting that TAAR5 might be involved in gaze stabilization, vestibular and motor control. Accordingly, in various behavioral tests TAAR5-KO mice demonstrated lower endurance but better coordination and balance compared to wild type mice. Furthermore, we found specific changes in striatal local field potentials and motor cortex ECoG such as а decrease in delta andan increase in theta oscillations of power spectra respectively. The data obtained suggest that TAAR5 plays a considerable role in the regulation of postural stability, muscle force, balance and motor coordination during active movements, likely via modulation of monoaminergic systems on different levels of sensorimotor control, including brainstem, cerebellum and forebrain.

Detection of VOR dysfunction during the gaze stabilization test: Does target size matter?

BACKGROUND: The Gaze Stabilization Test (GST) identifies vestibulo-ocular reflex (VOR) dysfunction using a decline in target recognition with increasing head velocity, but there is no consensus on target (optotype) size above static visual acuity. OBJECTIVE: To determine the optimal initial optotype size above static visual acuity to be used during the GST in subjects with unilateral vestibular dysfunction and healthy individuals. METHODS: Eight subjects with unilateral vestibular dysfunction (UVD) and 19 age-matched, healthy control subjects were studied with the standard GST protocol using two optotype sizes, 0.2 and 0.3 logMAR above static visual acuity (ΔlogMAR). Maximal head velocity achieved while maintaining fixation on both optotypes was measured. Sensitivity, specificity and receiver-operator characteristic area under the curve (ROC AUC) analyses were performed to determine the optimal head velocity cut off point for each optotype, based on ability to identify the lesioned side of the UVD group from the control group. RESULTS: There was a significant difference in maximal head velocity between the UVD group and control group using 0.2 ΔlogMAR (p = 0.032) but not 0.3 ΔlogMAR (p = 0.061). While both targets produced similar specificities (90%) for distinguishing normal from subjects with UVD, 0.2 ΔlogMAR targets yielded higher sensitivity (75%) than 0.3 logMAR (63%) and accuracy (86% vs 80%, respectively) in detecting the lesioned side in subjects with UVD versus controls with maximal head velocities≤105 deg/s (p = 0.017). Furthermore, positive likelihood ratios were nearly twice as high when using 0.2 ΔlogMAR targets (+ LR 10) compared to 0.3 ΔlogMAR (+ LR 6.3). CONCLUSION: The 0.2 ΔlogMAR optotype demonstrated significantly superior identification of subjects with UVD, better sensitivity and positive likelihood ratios than 0.3 ΔlogMAR for detection of VOR dysfunction. Using a target size 0.2logMAR above static visual acuity (ΔlogMAR) during GST may yield better detection of VOR dysfunction to serve as a baseline for gaze stabilization rehabilitation therapy.

Head movement kinematics are altered during gaze stability exercises in vestibular schwannoma patients

Gaze stability is the ability of the eyes to fixate a stable point when the head is moving in space. Because gaze stability is impaired in peripheral vestibular loss patients, gaze stabilization exercises are often prescribed to facilitate compensation. However, both the assessment and prescription of these exercises are subjective. Accordingly, here we quantified head motion kinematics in patients with vestibular loss while they performed the standard of care gaze stability exercises, both before and after surgical deafferentation. We also correlate the head kinematic data with standard clinical outcome measures. Using inertial measurement units, we quantified head movements in patients as they transitioned through these two vestibular states characterized by different levels of peripheral damage. Comparison with age-matched healthy control subjects revealed that the same kinematic measurements were significantly abnormal in patients both pre- and post-surgery. Regardless of direction, patients took a longer time to move their heads during the exercises. Interestingly, these changes in kinematics suggest a strategy that existed preoperatively and remained symmetric after surgery although the patients then had complete unilateral vestibular loss. Further, we found that this kinematic assessment was a good predictor of clinical outcomes, and that pre-surgery clinical measures could predict post-surgery head kinematics. Thus, together, our results provide the first experimental evidence that patients show significant changes in head kinematics during gaze stability exercises, even prior to surgery. This suggests that early changes in head kinematic strategy due to significant but incomplete vestibular loss are already maladaptive as compared to controls.

Mechanisms of punctuated vision in fly flight

ABSTRACTTo guide locomotion, animals control their gaze via movements of their eyes, head, and/or body, but how the nervous system controls gaze during complex motor tasks remains elusive. Notably, eye movements are constrained by anatomical limits, which requires resetting eye position. By studying tethered, flying flies (Drosophila) in a virtual reality flight simulator, we show that ballistic head movements (saccades) reset eye position, are stereotyped and leverage elastic recoil of the neck joint, enabling mechanically assisted redirection of gaze. Head reset saccades were of proprioceptive origin and interrupted smooth movements for as little as 50 ms, enabling punctuated, near-continuous gaze stabilization. Wing saccades were modulated by head orientation, establishing a causal link between neck signals and execution of body saccades. Furthermore, we demonstrate that head movements are gated by behavioral state. We propose a control architecture for biological and bio-inspired active vision systems with limits in sensor range of motion.

Sport-specific differences in dynamic visual acuity and gaze stabilization in division-I collegiate athletes

BACKGROUND: The vestibular-ocular reflex (VOR) integrates the vestibular and ocular systems to maintain gaze during head motion. This reflex is often negatively affected following sport-related concussion. Objective measures of gaze stability, a function mediated by the VOR, such as the computerized dynamic visual acuity test (DVAT) and gaze stabilization test (GST), may have utility in concussion management. However, normative data specific to sport, sex, or concussion history have not been established in collegiate athletes. OBJECTIVE: The objective of this study was to establish normative values for the DVAT and GST in collegiate athletes and explore the effect of sport, sex, and concussion history on VOR assessments. METHODS: The DVAT and GST were completed by 124 collegiate athletes (72 male, 52 female, mean±SD, age: 19.71±1.74 years, height: 173.99±13.97 cm, weight: 80.06±26.52 kg) recruited from Division-I athletic teams (football, soccer and cheerleading). The DVAT and GST were performed in the rightward and leftward directions during a single session in a standardized environment. Normative values for DVAT and GST measures were expressed as percentiles. Non-parametric statistics were used to compare differences between groups based on sex, sport, and concussion history. Alpha was set a-priori at 0.05. RESULTS: Overall, the median LogMAR unit for 124 athletes completing the DVAT was 0 (IQR = 0.17) for both leftward and rightward. The median velocities achieved on the GST were 145 °/sec and 150 °/sec (IQR = 45 and 40) for the leftward and rightward directions respectively. Significant differences were observed between sports (p = 0.001–0.17) for the GST with cheerleading demonstrating higher velocities than the other sports. However, no significant differences were identified based on sex (p≥0.09) or history of concussion (p≥0.15). CONCLUSIONS: Normative estimates for the DVAT and GST may assist in the clinical interpretation of outcomes when used in post-concussion evaluation for collegiate athletes. Although sex and previous concussion history had no effect on the DVAT or GST, performance on these measures may be influenced by type of sport. Sport-related differences in the GST may reflect VOR adaptations based on individual sport-specific demands.